SURVEY FOR ARMILLARIA BY PLANT ASSOCIATIONS IN NORTHERN ARIZONA
CHRIST W. HOFFMAN, ROBERT L. MATHIASEN, RICHARD W. HOFSTETTER, School of Forestry,
Northern Arizona University, Flagstaff, Arizona 86011;
MARY LOU FAIRWEATHER, Forest Health Protection, USDA Forest Service, Flagstaff, Arizona
86001;
JOHN D. SHAW, Interior West Forest Inventory and Analysis, USDA Forest Service, Ogden, Utah
84401;
JOHN W. HANNA, and NED B. KLOPFENSTEIN, Moscow Forestry Sciences Laboratory, Rocky
Mountain Research Station, USDA Forest Service, Moscow, Idaho 83843
ABSTRACT
Fungi in the genus Armillaria are associated with an important disease of deciduous and coniferous trees and shrubs
in western North America. This study examined the distribution of Armillaria by forest habitat types on the Kaibab
National Forest and northern Coconino National Forest, Arizona. Over 400 trees were examined for Armillaria in 76
Interior West Forest Inventory and Analysis permanent plots representing 17 different habitat types. Samples of the
fungus associated with Armillaria root disease were collected from 23 trees and identified using DNA sequencing. All
samples were determined to consist of a single species, Armillaria solidipes Peck [= A. ostoyae (Romagnesi) Herink].
Only 10 of the 76 plots and 5 of the 17 habitat types sampled had Armillaria solidipes present on one or more trees. A.
solidipes was more commonly found in mixed-conifer and subalpine forests and was rare in ponderosa pine (Pinus
ponderosa Doug. Ex. Larson & C. Larson) forests, which was consistent with previous root disease studies conducted
in the Southwest. However, our estimates of Armillaria presence may be conservative since we did not examine entire
root systems.
INTRODUCTION
Armillaria root disease has been commonly
associated with root decay and mortality of deciduous and coniferous trees and shrubs and has been
reported to affect more than 600 species of woody
plants (Garraway et al. 1991, Morrison et al. 1991).
This damaging root disease has been found in most
forests of the world, but it has been reported to be
more common and abundant in temperate and boreal
forests than in tropical regions (Kile et al. 1991). It
has been reported to occur in nearly every state of
the continental United States and also reported
widely in Canada and Mexico (Williams et al.
1986). This economically important tree disease has
been consistently associated with fungi in the genus
Armillaria (Fr.:Fr) Staude (Tricholomataceae),
hence the common name of the disease.
The classification of the genus Armillaria has
undergone a great deal of modification, but has now
been reported to contain approximately 40 species,
10 of which have been documented in North America (Watling et al. 1991, Brazee et al. 2012, RossDavis 2012, Volk 2013) (Table 1). Some species of
Armillaria reportedly survive as saprophytes in
woody substrates within soil or standing dead material, while others have been demonstrated to be
aggressive pathogens of living trees. The pathogenic
species can kill living roots, eventually killing the
infected tree, and then continue to live in dead material as saprophytes for several years (Kile et al.
1991). Species of Armillaria can be spread by sexually produced basidiospores, or spread vegetatively
by rhizomorphs and by transfer from infected roots
to healthy roots via contacts and/or grafts (Kile et al.
1991, Redfern and Filip 1991). Due to differences in
pathogenicity and host preferences among the different species of Armillaria found in North America, forest managers require precise information on
which species are present in different regions and
when possible, information on the probability that
Armillaria root disease is established in different
forest types and stands (McDonald et al. 1987, Kile
et al. 1991). Often trees infected with Armillaria
root disease have been stressed to the extent that
other agents, such as bark beetles, attack them and
can cause death of the trees (Miller and Partridge
1974, Tkacz and Schmitz 1986, Goheen and Hansen
1993). Therefore, it is common to observe mortality
caused by a complex of factors in forests infested
with this disease in Arizona (Wood 1983).
In the northern Rocky Mountains, the use of
habitat types (Daubenmire 1952) has been demonstrated to be a useful forest vegetation classification
system for predicting the environmental conditions
under which Armillaria root disease may be present
or absent in a stand (Williams and Marsden 1982,
McDonald et al. 1987, Byler et al. 1990, McDonald
1990, McDonald et al. 2005). The overall climatic
conditions influencing forest habitat types are correlated with predicting the occurrence of Armillaria.
HOFFMAN, C. W., R. L. MATHIASEN, R. W. HOFSTETTER, M. L. FAIRWEATHER, J. D. SHAW, J. W. HANNA, AND N. B. KLOPFENSTEIN. 2014.
SURVEY FOR ARMILLARIA BY PLANT ASSOCIATION IN NORTHERN ARIZONA. JOURNAL OF THE ARIZONA-NEVADA ACADEMY OF SCIENCE 45(2):76-86.
77
ARMILLARIA ROOT DISEASE IN NORTHERN ARIZONA g HOFFMAN ET AL.
Table 1. Species of Armillaria found in North America (Baumgartner and Rizzo 2001, Kim et al. 2010, Elias-Roman et al.
2013, Brazee et al. 2013, Nelson et al. 2013, Volk 2013).
Species
Distribution
Amillaria solidipes Peck/ostoyae (Romagnesi) Herink
Northern conifer zone, occasionally on hardwoods
A. gemina Bérubé & Dessurealt
Northeastern United States, eastern Canada
A. calvescens Bérubé & Dessurealt
Eastern Canada to Michigan and Wisconsin
A. sinapina Bérubé & Dessurealt
Northern conifer zone, but typically hardwoods in the East and
conifers in the West
A. mellea (Vahl:Fries) Kummer
Hardwood zone, mostly southeastern United States north to Iowa
and Wisconsin and south to Oklahoma, Texas, and Mexico. Eastern
distribution from Florida to the Appalachians to Québec. Known from
Arizona, California, and Oregon but not other areas of the West
A. gallica Marxmüller & Romagnesi
Hardwoods in South, Northeast, Midwest, and Mexico; Arizona,
California, and the Pacific Northwest
A. nabsnona Volk & Burdsall
Idaho, Washington, Oregon, Alaska, and British Columbia
A. cepistipes Velenovsky
Washington and British Columbia
A. tabescens (Scopoli) Emel
Southeastern United States into the Northwest, west to Ohio, also
farther west and north on shores of Great Lakes and south to
Veracruz, Mexico
A. altimontana Brazee, B. Ortiz, Banik & D. L.
Lindner
Idaho, Washington, Oregon, California, and British Columbia
In the northern Rocky Mountains, habitat types characterized as cold-dry or hot-dry environments were
found to be outside the ecological range of Armillaria
and excessively cold or moist sites may also limit the
growth and development of Armillaria and hence
have little of the fungus present (McDonald et al.
1987). In the Southwest, where many of the forests
are characterized by hot-dry or warm-dry climatic
conditions, Armillaria root disease is considered
important only on more mesic sites (Wood 1983).
However, in northern Arizona few studies have been
conducted to examine the distribution of Armillaria
or identify the species of Armillaria present using the
currently recognized classification of the genus. In
the Southwest, habitat types are often called plant
associations (Stuever 1997) and we have adopted this
terminology since the two terms are synonymous.
Historically, Armillaria root disease was thought
to be caused by a single species, Armillaria mellea
(Vahl:Fr.) Kummer. Although Wood (1983) applied
the concept of using Armillariella in place of
Armillaria in a study in the southwestern United
States, the use of the previous genus was invalidated
by Watling et al. (1982) and is no longer used as an
obligate synonym for Armillaria (Volk 2013).
Under the current classification system for Armillaria,
the distribution of A. mellea is confined to the eastern
and midwestern United States and California (Volk
2013). However, A. mellea was reported from southeastern Arizona on oaks (Quercus spp.) by Gilbertson and Bigelow (1998) based on morphology, and
recently confirmed (Nelson et al. 2013). The primary species of Armillaria associated with a root
disease of conifers throughout the western United
States has now been designated as A. solidipes Peck
[=A. ostoyae (Romagnesi) Herink] (Burdsall and
Volk 2008), pending a vote for nomenclatural conservation (Hunt et al. 2011), and was the species
morphologically identified in a study in New Mexico
(Omdal et al. 1995). Gilbertson and Bigelow (1998)
also reported A. solidipes (as A. ostoyae) in the Sky
Islands of southeastern Arizona on several conifers
and quaking aspen (Populus tremuloides Michx.).
However, the identification of Armillaria species
that occur in Arizona using DNA-based techniques
is needed, as well as additional information on the
distribution and abundance of Armillaria in the
northern part of the state.
ARMILLARIA ROOT DISEASE IN NORTHERN ARIZONA g HOFFMAN ET AL.
Today it is possible to identify species of
Armillaria using DNA sequencing techniques (Kim et
al. 2006, Ross-Davis et al. 2012). Kim et al. (2006)
examined rDNA sequences for three regions and
used amplified fragment length polymorphisms
(AFLPs) to assess the phylogenetic relationships of
several species of Armillaria. They concluded that
ribosomal DNA intergenic spacer sequences
(IGS-1) and AFLP genetic markers could be used to
potentially distinguish the North American species
of Armillaria. In addition, the phylogenetic relationships among 15 globally diverse Armillaria species
and eight Japanese species were examined and separated using partial sequences of the translation
elongation factor-1 alpha (tef-1α) gene (Maphosa et
al. 2006, Hasegawa et al. 2010). DNA based identification of Armillaria has also been used in North
America and can now confidently differentiate
species (Ross-Davis et al. 2012). Five clades have
been identified using the tef-1α gene which clearly
separated the North American species of Armillaria.
Therefore, current molecular methods have been
shown to be effective at correctly identifying the
currently recognized North American species of
Armillaria (Ross-Davis et al. 2012).
Because little information was available on the
species of Armillaria that occur in northern Arizona,
the hosts affected, or the distribution of the pathogen by forest type or plant association, this study
was initiated in 2011 in cooperation with USDA
Forest Service: Rocky Mountain Research Station
(RMRS); Interior West Forest Inventory and Analysis program (IW-FIA); and Forest Health Protection, Southwest Region. Permanent plots established
by IW-FIA on the Kaibab and Coconino National
Forests, Arizona, were used as sampling sites. These
plots were used because they allowed the accomplishment of several ancillary goals: 1) this study
served as a pilot test of methodology that could
potentially be added to FIA protocols, 2) because
the FIA program uses a systematic sampling design,
the results of this study can be used to estimate the
proportion of area with Armillaria present, and 3)
because the plots are part of a continuous forest
inventory and monitoring system, the results can
serve as a baseline for future comparisons.
Plots representing 17 plant associations on three
ranger districts were surveyed, in which dead and
living trees with or without root disease symptoms
were examined for the presence of Armillaria.
Samples of Armillaria were collected when observed and sent to the RMRS Forestry Sciences
Laboratory in Moscow, Idaho, for positive identification based on DNA sequences of partial Large
Subunit and intergenic spacer 1 (LSU-IGS1) regions
of ribosomal DNA and tef-1α. Here we report our
78
findings, which support previous reports that Armillaria root disease is not common in northern
Arizona and that the disease is commonly associated
with only one species of Armillaria.
METHODS
This study used permanent plots established by
the IW-FIA program on the Kaibab and Coconino
National Forests in northern Arizona. Plots on the
North Kaibab, Williams, and Flagstaff Ranger Districts were selected based on ownership, accessibility, and plant association. A total of 76 plots were
sampled that represented 17 forest plant associations
(Table 2 and Fig. 1). Rather than splitting plant
associations into phases, plots representing a phase
were grouped under each major plant association
sampled. Plots were visited during the summers of
2011 and 2012.
Plots established by IW-FIA consist of four circular subplots (radius 7.3 m, 0.02 ha) (USDA Forest
Service 2011) (Fig. 2). Each unit has a central subplot with three additional subplots established
36.6 m from its center at azimuths of 360°, 240°,
and 120°. Each sampling unit was classified by elevation, aspect, forest type, soil type, and plant
association. Standard forest inventory data collected
from the four subplots included trees species,
diameter breast height (dbh, 1.4 m above the
ground), tree heights, and information on downedwoody material. To avoid disturbance associated
with surveys for Armillaria within the IW-FIA
subplots, circular supplemental plots (0.04 ha) were
established 36.6 m from the center of the central
IW-FIA subplot at an azimuth of 300° (Fig. 2). Only
one supplemental plot was established for each set
of IW-FIA subplots sampled.
In each supplemental subplot, one live or dead
tree of each species present in the plot was examined
for the presence of Armillaria by each of the following dbh classes: <20, 20-40, and >40 cm whenever
possible. At least three trees were examined in each
plot. Dead trees or live trees with symptoms of root
disease were given priority for examination over live
trees with no root disease symptoms. Only the
species and diameter (dbh, nearest cm) of trees sampled for the presence of Armillaria were recorded for
each supplemental plot. Examination of trees for the
presence of Armillaria was conducted by excavating
at least one main root to a radial distance of 0.8 m
from the bole. When mycelia fans were present on
roots, samples were collected by carefully removing
a section of the infected root so the integrity of the
bark remained intact. The size of sampled root sections or mycelia fans varied depending on the size of
the infected root or bole. Up to three samples were
collected from each infected tree. Root samples that
79
ARMILLARIA ROOT DISEASE IN NORTHERN ARIZONA g HOFFMAN ET AL.
Table 2. Number of plots surveyed and number of plots with Armillaria by plant association on the Flagstaff Ranger District, Coconino National Forest and the North Kaibab and Williams Ranger Districts,
Kaibab National Forest, Arizona. Plant association acronyms (e.g., PSME/FEAR) and plant species
classications follow Stuever (1997).See Appendix 1 for a list of common and scientific names of plants
used in the name of plant associations.
Ranger district
Flagstaff
Williams
North Kaibab
Total
Number
of plots
Plots with Amillaria
Subalpine fir/Nevada pea (ABLA/LALAL3)
1
0
White fir/Creeping barberry (ABCO/MARE11)
1
0
Douglas-fir/Arizona fescue (PSME/FEAR)
2
0
Douglas-fir/Creeping barberry (PSME/MARE11)
1
0
Douglas-fir/Gambel oak (PSME/QUGA)
1
1
Ponderosa pine/Arizona fescue (PIPO/FEAR)
7
1
Ponderosa pine/Blue grama (PIPO/BOGR2)
7
0
Ponderosa pine/Mountain muhly (PIPO/MUMO)
5
0
Douglas-fir/Mountain muhly (PSME/MUMO)
1
0
Ponderosa pine/Arizona fescue
7
0
Ponderosa pine/Blue grama
3
0
Ponderosa pine/Mountain muhly
2
0
Subalpine fir/Common juniper (ABLA/JUCO6)
5
3
Engelmann spruce/Fleabane (PIEN/EREX4)
3
0
Engelmann spruce/Maple (PIEN/ACGL)
1
0
Blue spruce/Dryspike sedge (PIPU/CAFO3)
4
2
Blue spruce/Fleabane (PIPU/EREX4)
1
0
White fir/Arizona fescue (ABCO/FEAR)
2
0
White fir/Creeping barberry
4
2
White fir/Dryspike sedge (ABCO/CAFO3)
3
0
Douglas-fir/Arizona fescue
1
0
Douglas-fir/Gambel oak
1
0
Ponderosa pine/Arizona fescue
4
1
Ponderosa pine/Blue grama
2
0
Ponderosa pine/Mountain muhly
3
0
Ponderosa pine/Gambel oak (PIPO/QUGA)
4
0
76
10
Plant association
ARMILLARIA ROOT DISEASE IN NORTHERN ARIZONA g HOFFMAN ET AL.
Figure 1. Approximate locations of 76 plots surveyed for Armillaria on the Kaibab and Coconino National Forests, Arizona.
80
81
Figure 2. Plot design for Intermountain West Forest Inventory
and Analysis sample plots with the supplemental Armillaria
plot placed at a 300E azimuth from the center of the plot
cluster.
appeared to be colonized by Armillaria were collected from 42 trees. Each Armillaria sample was
placed in a paper bag and all the bags collected for
a tree were placed in a Ziploc bag and kept in a
cooler while in the field and then refrigerated.
Within 2 weeks, samples were mailed overnight
on ice to the RMRS Forestry Sciences Laboratory,
Moscow, Idaho. Armillaria was isolated from mycelial fans, rhizomorphs, or wood; then established in
culture on 3% malt-agar medium (3% malt extract,
1.5% peptone, 3% glucose, and 1.5% agar) and
incubated at 22EC in the dark. Template DNA was
collected directly from scrapings of actively growing mycelia or by using DNeasy Plant Mini DNA
extraction kits (Qiagen Inc., Valencia, CA, USA) to
extract DNA from ca. 100 mg of mycelia that was
cultured on 0.2-µm-pore nylon filters (Millipore
Corp., Billerica, Massachusetts, USA) overlaying
the culture medium. Extracted DNA samples were
used for PCR and sequencing of the partial Large
Subunit and intergenic spacer 1 (LSU-IGS1) regions
of the ribosomal DNA was used to identify which
species of Armillaria was associated with each
sample (Kim et al. 2006). Species identify was
confirmed using the tef-1α gene (Ross-Davis et al.
2012). Armillaria sequences were identified based
on similarity (>95%) and phylogenic placement
using SplitsTrees4 with default parameters (Huson
and Bryant 2006) when compared against reference
sequences from Kim et al. (2006), Hanna et al.
(2007), Ross-Davis et al. (2012) and/or EliasRoman et al. (2013).
RESULTS
A total of 76 supplemental 0.04-ha plots were
inspected for Armillaria representing 17 plant
ARMILLARIA ROOT DISEASE IN NORTHERN ARIZONA g HOFFMAN ET AL.
associations (Table 2). A total of 10 plots had one or
more trees with Armillaria: 8 of these plots were on
the North Kaibab Ranger District (Kaibab Plateau)
and two were on the Flagstaff Ranger District
(Table 2 and Fig. 1). This represented 21% and 8%
of the plots surveyed on those districts, respectively.
Armillaria was not detected on the Williams Ranger
District. A single FIA plot in Arizona has an expansion factor of approximately 2,500 ha, depending on
the actual number of plots surveyed at a given point
in the inventory cycle. Therefore, the simplified
estimate is that the survey area of this study was
approximately 190,000 ha, at least 25,000 ha (13%)
of which would be expected to have Armillaria
present. However, our estimates of Armillaria presence may be conservative since we did not examine
entire root systems.
Armillaria was found in 5 of the 17 plant associations sampled. It was most often found in plant
associations that represented warm-dry climatic
conditions of the subalpine or mixed-conifer forest
types (Stuever 1997); the subalpine fir/common
juniper (ABLA/JUCO6), white fir/creeping barberry
(ABCO/MARE11), and Douglas-fir/Gambel oak
(PSME/QUGA) plant associations (Tables 2 and 3).
Armillaria was also detected in one plant association that represented cold-wet climatic conditions
of the mixed conifer forest type; the blue spruce/
dryspike sedge (PIEN/CAFO3) plant association.
Although 11 plots were sampled that represented
three additional subalpine (PIEN/ACGL, PIEN/
EREX4, and ABLA/LALAL3) and four mixed conifer forest plant associations (PIPU/EREX4, ABCO/
FEAR, ABCO/CAFO3, and PSME/MUMO),
Armillaria was not detected in any of them (Table
2). Armillaria was only found in one ponderosa pine
plant association, ponderosa pine/Arizona fescue
(PIPO/FEAR), and although 18 plots were sampled
for this plant association, the pathogen was only
found in two plots; one each on the Kaibab and
Coconino National Forests (Table 2). Although 25
plots representing three other ponderosa pine plant
associations (PIPO/BOGR2, PIPO/MUMO, and
PIPO/QUGA) were sampled, Armillaria was not
detected.
A total of 343 conifers and 82 deciduous
species were surveyed in the 76 plots that were
examined for Armillaria (Table 4). Of these, only
19 conifers and four quaking aspen had evidence of
Armillaria (mycelial fans) on their roots or main
boles that were detected by the survey method used.
Rhizomorphs were rare with only two short segments collected from the bark of mycelial fan samples. The distribution of the 425 trees examined for
Armillaria by diameter classes was: <20 cm – 239
trees; 20-40 cm – 117 trees; >40 cm – 69 trees. Of
ARMILLARIA ROOT DISEASE IN NORTHERN ARIZONA g HOFFMAN ET AL.
82
Table 3. Number of trees surveyed (first number) and number of trees with Armillaria (second number) by tree species for the five plant associations where Armillaria was observed. Plant association
acronyms follow Stuever (1997) and see Table 2.
Ponderosa
pine
Quaking
aspen
Douglas-fir
White fir
Engelmann
spruce
Blue
spruce
PIPO/FEAR
44/3
0/0
0/0
0/0
0/0
0/0
PSME/QUGA
4/1
3/3
2/0
0/0
0/0
0/0
ABCO/MARE11
11/2
9/0
9/1
6/2
0/0
2/0
PIPU/CAFO3
7/3
6/0
0/0
3/0
3/2
3/0
ABLA/JUCO6
11/1
14/1
10/2
6/0
12/2
0/0
Total
76/10
32/4
21/3
15/2
15/4
5/0
Plant association
the 23 trees in which Armillaria was detected,
Table 4. Number of trees surveyed and number of trees and per11 were in the <20 cm class, 10 were in the
centage with Armillaria by tree species in 76 plots on the Kaibab
20-40 cm class, and two were in the >40 cm
and Coconino National Forests, Arizona.
class. Armillaria was detected primarily on
Number with Percent with
Number
dead trees; 19 of the 23 trees (83 %).
Tree
species
examined
Armillaria
Armillaria
The two most commonly surveyed tree
species were ponderosa pine (Pinus
Ponderosa pine
189
10
5
ponderosa Dougl. ex Larson & C. Larson) and
quaking aspen. Both of these species were
Quaking aspen
65
4
6
infrequently associated with Armillaria; it was
found on only 10 ponderosa pines (5%) and
Douglas-fir
46
3
7
four aspen (6%) (Table 4). Four other conifers
White fir
43
2
5
that were sampled in the subalpine and mixedconifer plant associations were Douglas-fir
Engelmann spruce
27
4
15
(Pseudotsuga menziesii (Mirb.) Franco), white
fir (Abies concolor (Gord. & Glend.)
Blue spruce
20
0
0
Hilldebr., Engelmann spruce (Picea
Gambel oak
11
0
0
engelmannii Parry ex Engelm.), and blue
spruce (Picea pungens Engelm.). Armillaria
Utah juniper
7
0
0
was also detected on three of these species and
the incidence of infection was again very low:
Colorado pinyon pine
6
0
0
Douglas-fir (7 %), white fir (5 %), and Engelmann spruce (15 %) (Table 4). Only a few
Limber pine
4
0
0
trees of the following species were examined
New Mexico locust
6
0
0
for Armillaria within the sample plots and the
pathogen was not detected: Gambel oak
Subalpine fir
1
0
0
(Quercus gambelii Nutt.), New Mexican
locust (Robinia neomexicana Gray), Utah
Total
425
23
5
juniper (Juniperus osteosperma (Torr.) Little),
Colorado pinyon pine (Pinus edulis Engelm.),
limber pine (Pinus flexilis James), and
subalpine fir (Abies lasiocarpa (Hook.) Nutt.).
DISCUSSION
Based on DNA sequences of the LSU-IGS1 and
Recently, it was determined that A. solidipes
the tef-1α gene, isolates from the 23 trees were all
was the appropriate name for the species associated
identified as Armillaria solidipes (= A. ostoyae).
with Armillaria root disease of conifers in the West
(Burdsall and Volk 2008); however, Hunt et al.
83
(2011) argued that A. solidipes is an ambiguous
species which is probably not conspecific with A.
ostoyae and as a result have proposed that A.
ostoyae be conserved over A. solidipes. Thus, the
appropriate taxonomy for the Armillaria sp. that
was recovered in this study remains controversial.
Other species of Armillaria that have been reported
in Arizona include A. mellea and A. gallica
Marxmüller & Romagnesi. The reports of A. mellea
have been from the Chiricahua, Pinaleno, Santa
Catalina, and Santa Rita Mountains in southeastern
Arizona on three species of oak (Gilbertson and
Bigelow 1998) and the report of A. gallica is from
the Mogollon Rim on Douglas-fir in north-central
Arizona (Nelson et al. 2013). Other species of
Armillaria that are of interest in Arizona include A.
sinapina (Table 1) and a recently discovered undescribed species from the State of Mexico, Mexico
(Elias-Roman et al. 2013). However, it is improbable that these taxa are the common species of
Armillaria associated with root disease in northern
Arizona based on our results, but further sampling
may discover that these other species are more
common than what our findings suggest.
Armillaria solidipes can be highly pathogenic
on conifers throughout the western United States,
but we also found it infecting aspen in subalpine
forests on the north Kaibab Plateau and in mixed
conifer forests on the San Francisco Peaks.
Armillaria was most often found on dead trees and
was probably associated with mortality of the
infected trees. However, insects that attack weakened trees (particularly bark beetles of conifers)
may have also contributed to their death. Mortality
of ponderosa pine in northern Arizona has been
shown to sometimes involve a complex of Armillaria root disease and bark beetles (Dendroctonus
spp. and Ips spp., Scolytidae) or dwarf mistletoe
(Arceuthobium spp., Viscaceae), or both (Wood
1983). However, we did not examine trees for the
presence of insects or other diseases. Armillaria
solidipes generally exists as both a pathogen and a
saprophyte, but can exist in a nonpathogenic state in
some forests (Redfern and Filip 1991). However,
since we primarily found Armillaria associated with
dead trees that displayed symptoms of disease, the
populations we sampled in northern Arizona are
considered pathogenic and likely contributed to the
death of the infected trees.
In comparison to the northern Rocky Mountains, northern Arizona evidently has a relatively
low incidence of Armillaria root disease. McDonald
et al. (1987) reported they found Armillaria associated with over 30% of each tree species they sampled in Washington, Idaho, and Montana. Our
results found that the incidence of Armillaria on the
ARMILLARIA ROOT DISEASE IN NORTHERN ARIZONA g HOFFMAN ET AL.
trees we examined was only 15% or less. Wood
(1983) also found a relatively low incidence of
Armillaria root disease in Arizona. The highest incidence of the disease he reported for Arizona was for
mixed conifer/spruce-fir forests on the ApacheSitgreaves National Forest where 24% of the dead
trees he examined were infected with Armillaria.
Wood (1983) only reported that 1, 7, and 12%
of the dead ponderosa pines examined on the Kaibab, Apache-Sitgreaves, and Coconino National
Forests, respectively, had Armillaria root disease. In
New Mexico, he only found Armillaria root disease
on 8% of the dead ponderosa pines surveyed on the
Carson and Santa Fe National Forests. Our results
also demonstrate a relatively low incidence of
Armillaria on ponderosa pine in northern Arizona.
This was particularly evident in the ponderosa pine
habitat types sampled where A. solidipes was only
found on 3 of the 110 ponderosa pines we surveyed;
all 3 were in the PIPO/FEAR plant association
(Table 3). Most of the infected ponderosa pines we
observed (6 of 10 trees) were in mixed conifer
forests. McDonald et al. (1987) hypothesized that
Armillaria was probably completely absent from the
ponderosa pine and limber pine plant associations in
the northern Rocky Mountains. Our results indicated that Armillaria may also be absent from, or at
least rare in, most ponderosa pine plant associations
in northern Arizona, but additional surveys are
needed in these plant associations because our sample sizes were relatively small compared to those of
McDonald et al. (1987).
Wood (1983) reported that 38% of the dead
trees examined in the subalpine forests and 15% of
the dead trees in the mixed-conifer forests of New
Mexico had Armillaria root disease. Although we
did not survey a large number of plant associations
(4) or plots (10) in the subalpine forests of northern
Arizona, the incidence of Armillaria was the highest
(11% of the trees examined) in one of the plant
associations (ABLA/JUCO6) compared to the other
plant associations surveyed (PIEN/ACGL, PIEN/
EREX4, and ABLA/LALAL3). We also found
Armillaria in three mixed-conifer forest plant
associations (ABCO/MARE11, PSME/QUGA, and
PIEN/CAFO3). This suggested that additional sampling should be completed in the subalpine and
mixed-conifer forests of northern Arizona, particularly on the Kaibab Plateau where Armillaria has
been observed to be more common in those forest
types than in the ponderosa pine type (Wood 1983).
Of the 38 plots we surveyed on the Kaibab Plateau
in subalpine and mixed conifer forests, 21% were
infested with Armillaria. In addition, we found that
15% of the Engelmann spruce examined were
infected with Armillaria, which was the highest
ARMILLARIA ROOT DISEASE IN NORTHERN ARIZONA g HOFFMAN ET AL.
incidence of infection for a tree species surveyed.
Therefore, it would be worthwhile to sample additional habitat types dominated by Engelmann spruce
to better determine the incidence of Armillaria in
subalpine and mixed-conifer forests elsewhere in
Arizona. Our results and those reported by Wood
(1983) and McDonald et al. (1987) have demonstrated that Armillaria is evidently more prevalent
in mixed-conifer and subalpine forests than it is in
ponderosa pine forests and this relationship should
be investigated in other regions of the West.
The methodology used in this study has potential for use in the FIA inventory and monitoring
program. The use of an additional subplot, along
with the survey/sampling methods used, allows for
application of this sampling protocol with little concern about adverse impact to the regular FIA plot
footprint. Expanded employment of this methodology would permit statistically valid estimation of
the minimum area with Armillaria present, as well
as the ability to estimate change in the area infested
by Armillaria over time. Future surveys using IWFIA plots could use two, or possibly three,
supplemental 0.04 ha plots which would increase
the accuracy for estimates of the presence of
Armillaria, yet continue to minimize the disturbance
to the sampling site.
ACKNOWLEDGMENTS
We appreciate the Arizona Game and Fish Department allowing the use of housing on the North Kaibab
Plateau. This study was funded by the Mission Research
Program, School of Forestry, Northern Arizona University; the Special Technology Development Program,
Forest Health Protection, USDA Forest Service; and
Forest Inventory and Analysis, USDA Forest Service.
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ARMILLARIA ROOT DISEASE IN NORTHERN ARIZONA g HOFFMAN ET AL.
Appendix 1. Common and scientific names of plants used for plant associations
(Stuever 1997).
Common name
Scientific name
corkbark fir (subalpine fir)
Abies bifolia A.Murray (Abies lasiocarpa (Hooker) Nuttall)
white fir
Abies concolor (Gordon & Glendinning) Hildebrand
Engelmann spruce
Picea engelmannii Parry ex Engelmann
blue spruce
Picea pungens Engelmann
ponderosa pine
Pinus ponderosa Douglas ex Lawson & C. Lawson
Douglas-fir
Pseudotsuga menziesii (Mirbel) Franco
Gambel oak
Quercus gambelii Nuttall
Rocky Mountain maple
Acer glabrum Pursh
common juniper
Juniperus communis L.
creeping barberry
Mahonia repens (Lindley) G. Don
Nevada pea
Lathyrus lanszwertii Kellog
blue grama
Bouteloua gracilis (Kunth) Griffiths
Arizona fescue
Festuca arizonica Vasey
mountain muhly
Muhlenbergia montana (Nuttall) Hitchcock
fleabane
Erigeron eximius Greene
dryspike sedge
Carex foenea Willdenow
86